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Direct Measurement of Bronchial Arterial Flow By BRUNO HORISBERGER, M.D., AND SIMON EODBARD, M.D., T Downloaded from http://circres.ahajournals.org/ by guest on June 17, 2017 in 30 dogs, found that the bronchial arteries arise in all cases from the first to the fourth right aortic intercostal arteries. Miller13 showed that the bronchial arteries supply the airways as far as the respiratory bronchioles. Branches to the subpleural capillary network on the surface of the lung, to the vasa vasoruin of the larger pulmonary vessels, and to the mediastinal structures were also demonstrated. A curiosity of the true bronchial circulation is the fact that it has no veins of its own. Liebow and his group14 studied the venous drainage of the bronchial vascular bed and pointed out that the intrapulmonary drainage is via the pulmonary veins to the left heart. The extrapulmonaiy part of the bronchial vascular bed drains mainly via the azygos vein and the superior vena eava into the right heart. The "bronchial" arteries, therefore, represent a vascular system which supplies numerous mediastinal structures in addition to the bronchial tree. Many attempts utilizing both indirect and direct methods have been made to measure tlie flow through this system. Indirect measurements were made after ligation of the pulmonary artery to one lung in dogs (Bloomer, Harrison, Lindskog, and Liebow,"' and Vidoue and Liebow15). The collateral flow participating iu gas exchange ("effective" flow) was computed by bronchospirometry together with the Fick principle and was found to be about 300 ml./min./M.2 of body surface. Since the method cited appraises only the part of the bronchial flow which participates in gas exchange, the values reported are surprisingly high. The Fick principle has been used to ineassure the "effective" pulmonary collateral blood flow in man (Fishman et al. 8 ). In longstanding intrinsic lung disease with increased pulmonary vascular resistance, the effective collateral flow is known to be increased, but even so it is less than 10 per cent of the HE normal bronchial arterial blood flow provides only a very small portion of the blood flow through the lungs.1' 2 Since it supplies oxygen and nutrients to the bronchial musculature and mucosa, it may have importance for pulmonary mechanisms far beyond that expected on the basis of its small flow. After giving up its oxygen on passage through the pulmonary parenchyma, this flow passes into the pulmonary system where it may contribute oxygen-depleted blood to the pulmonary venous outflow. Precapillary anastomoses probably play a minimal role under normal circumstances.3'4 Because of the great potential for proliferation of the bronchial vascular system in congenital anomalies and inflammatory conditions, and after experimental obstruction of the pulmonary artery,5' ° the flow through this system may also have relevance in the evaluation of circulatory mechanisms. The normal anatomy of the nutrient arteries supplying the parenchyma of the lung was studied long ago by Leonardo da Vinci,7 von Haller,8 and Kiittner.9 The great variability in the topographical origin was early recognized. Cockett and Vass10 have reviewed the pertinent literature. Kiittner9 demonstrated that dye injections into the aorta resulted in the staining of the bronchial mucosa in man; he described the posterior bronchial arteries in the dog and showed that the branches to the right and left lung often had a common trunk with a medial intercostal artery, emerging from the aorta at the sixth thoracic segment. Berry et al.11 confirmed the arrangement desci'ibed by Kiittner. Notkovich,12 in an extensive study From the University of Buffalo Chronic Disease Research Institute, Buffalo, N. T. Dr. Horisberger's present address: University of Zurich, Switzerland. Supported in part by the Now York State Department of Health and by Grant H-2271 (C3) from the National Heart Institute of the U. S. Public Health Service. Received for publication May 12, 1960. Circulation Research, Volume VIII, November 19t>0 PH.D. 1149 1150 Downloaded from http://circres.ahajournals.org/ by guest on June 17, 2017 cardiac output. The collateral flow approaches normal cardiac output values only in cases of congenital absence of the pulmonary artery. The bronchial artery flow in dogs was measured directly by Bruner and Schmidt16 who supplied femoral arterial blood to a cannula in the origin of the right bronchial artery at the fifth intercostal space. A bubble flowmeter showed a range of delivery of 0.6 to 27 ml./ min. with an average of 4 ml./min. Labeled erythrocytes showed that the right lung rereived two-thirds of the bronchial arterial blood while the remainder supplied the mediastinum. Stimulation of the vagus increased flow to the bronchial vascular bed, while sympathetic stimulation reduced the flow. "Williams and Towbin17 ligated the pulmonary artery and then estimated bronchial flow as the backflow from the cut distal segment of the vessel. They found this to be 4 to 9 ml./ min. More recently, State et al.1 and Cudkowicz et al.2 measured the left and right heart output simultaneously in dogs and calculated the difference, i.e., the collateral flow, to be approximately 1 per cent of the total cardiac output. To obtain further insights into the regulation of the bronchial arterial circulation, we have developed a method which registers flow continuously in dogs. This technic permits direct and continuous measurement of the changes due to experimental procedures or to the administration of drugs. Methods It is difficult to isolate the true bronchial arteries from their widespread anastomoses with the mediastinal and pericardial vessels. However, a technic was developed in the course of the preliminary studies in a series of 12 dogs by means of which the extrabronehial fraction of flow could be minimized. This teehnic has since been used with only slight variations in more than 20 experiments. Ten dogs were anesthetized with intravenous injection of pentobarbital sodium (about 30 mg./ Kg.). A large cannula was tied into the trachea through a low incision. The cervical vagus nerves were isolated. To abolish spontaneous respiratory movements, a continuous infusion of diacetylcholine chloride (succinyleholine) (0.16 mg. in HORISBERGER, RODBARD 2 ml. saline/min.) was administered intravenously. Intermittent positive pressure breathing was maintained at a selected insufflation pressure, using a Burns valve.18 After a left thoracotomy, the sixth rib was resected. The first 5 lateral and the first medial intercostal arteries were then ligated at the aorta. The descending aorta was retracted venkally and the second, third, and fourth medial intercostal arteries were then isolated. The posterior bronchial arteries usually originated at the second and third medial intercostal arteries at the fifth right intercostal space. Occasionally, the bronchial artery for the left lung originated directly from the aorta. After the bronchial vessels were isolated, the remaining medial intercostal arteries down to the fifth branch were ligated. The esophageal branches were ligated. The segment of the aorta from the second to the fourth intercostal artery, which contained the vessels to the pleura, mediastinum, and bronchial tree, i.e., the bronchial vessels, was then isolated to produce a small vascular sac. The gap in the descending aorta was bypassed by means of a T-tube. One arm of the T-tube was connected to a rotameter (Fisher and Porter Co., No. O2.F1/ 8-20-5/36) and then to the isolated aortic segment (%• 1). Plastic cannulas, 1 mm. in diameter, were tied into the pulmonary artery and into a left pulmonary vein. Simultaneous pressure recordings taken from these vessels as well as from the tracheal tubes were traced on a Sanborn direct writing apparatus. The bronchial vascular resistance (R) was calculated as the pressure drop (AP) in mm. Hg from aorta to pulmonary vein, divided by the quantity (Q) of flow in ml. blood per minute so that AP R = Q At the end of each experiment, 15 0.1 per cent solution of "fast green" injected into the aortic sac to visualize lar communications and the tissues it ml. of a dye were its vascusupplied. Results Characteristics of Flowmeter and Preparation The flowmeter (capacity 0 to 60 ml./min.) had a curvilinear characteristic for flows less than 5 ml./min., and was quite linear in the 5 to 60 ml. range. The pressure drop across the flowmeter between the aorta and the bronchial arterial system was less than 5 mm. Hg and the phase of the pulse pressure curve was practically unchanged (fig. 2). The perfusion pressure and phase relationships for Circulation Research, Volume VIII, November 1960 BEONCHIAL ARTERIAL FLOW 1151 Cm Hf Ai AORTA M00 UGATED NTERCOSTAL 30 20 A SEGMENT OF AORTA PA 10 S0C Downloaded from http://circres.ahajournals.org/ by guest on June 17, 2017 Figure 1 Essentials of the preparation. Respiratory gases were supplied from commercial cylinders to a series of reduction valves (upper left) which lowered the insufflation pressure to a selected value, usually 20 cm. water. The gas then passed through a Burns valve to the trachea. The bronchial blood supply is shown at the right. Aortic blood passes through a flowmeter to the isolated aortic segment from which the branches to the bronchial arteries originate. The crossmarks on the lines to the esophagus and intercostals indicate that these vessels have been ligated. The "bronchial" arteries supply the bronchial tree and both lungs, as well as the mediastinum. the bronchial arterial system were therefore practically identical with the central aortic pressure. This could be achieved because the orifices of the bronchial arteries were not cannulated and no significant additional resistance was introduced by our preparation. Flow Measurements Initial Reduction Blood flow measurements were recorded at intervals of 10 to 30 seconds. The bronchial blood flow was highest immediately after it had been interrupted for several minutes during the preparation of the aortic sac and the connection of the fiowmeter, and then fell to a constant level within the course of a few minutes (fig. 3). Spontaneous Variations Small spontaneous variations in bronchial artery flow were sometimes seen in our experiments. One of our dogs showed larger variation for a prolonged period of time, but these Circulation Research, Volume VIII, November 1960 Figure 2 Pressure contour and phase relationship of the pulse loave in the Aorta (A,) aiid in the sac (At) were not altered by the intervention of the flowmeter, and the pressure drop xuas negligible. Calibration marking are in mm. Hg; PA refers to the pressure in the pulmonary artery. were synchronous with marked fluctuations in systemic blood pressure due to arrhythmias. Effects of Air Pressure An increase from 20 to 30 cm. water insufflation pressure was associated with an increase in the calculated bronchial vascular resistance in 4 dogs (fig. 3). This was indicated by a fall in flow; a decrease in insufflation pressure to 20 cm. water was then accompanied by a return of the blood flow to previous values. Further lowering of the insufflation air pressure did not produce a further decrease in bronchial vascular resistance in our preparations. Vagotomy After the bronchial flow was stable for at least 5 minutes, the previously isolated vagi were cut bilaterally in dogs 4 to 8. The calculated bronchial vascular resistance increased within a few seconds in all 5 animals, and then persisted at the higher values (table 1). l-epinephrine When the systemic pressure increased after intravenous injection of Z-epinephrine, the flow through the bronchial vascular system increased proportionate!y. Injections of Z-epinephrine into the bronchial artery via the 1152 HORISBERGER, RODBARD Table 1 Effect of Bilateral Vagotomy on Bronchial Vascular Resistance Before vagotomy After vagotomy Resist. PVP Dog 4 5 G 7 8 Aortic BP mm. Hg mm. Hg 135 120 125 80 100 Flow ml./min. 4 8 6 9.0 25.3 4.0 O 3.0 35.0 s PVP Flowmm. Hg Aortic BP mm. Hg mm. Hg mi./min. ml./min. 14.6 4.4 29.8 26.0 2.6 200 135 130 90 100 7 9 6 10.0 15.5 3.0 3.0 30.5 O 8 Resist. mm. Hg ml./min. 19.3 8.1 41.3 29.3 3.0 Change in vascular resistance (%) + 32. +S4. +39. +13. +12. BP = Blood pressure. PVP = Pulmonary venous pressure. BP-PVP = Pressure gradient (BP) across the pulmonary vascular system. Resistance is calculated as /\P/flo\v. Downloaded from http://circres.ahajournals.org/ by guest on June 17, 2017 Table 2 Effect of Serotonin on Bronchial Vasiular Resistance Dog 4 (vagotomized) "i (vagotomized) S 9 10 Paor. 150 160 130 135 100 90 90 105 110 Flow before serotonin Q *Vv 7 G S 9 3 O 9 9 9.0 10.0 14.5 13.5 3.0 3.0 3.0 4.0 4.5 Peak flow R 15.8 15.4 8.4 9.3 32.3 29.3 29.3 25.8 24.0 p * aor. P,., Q R AR% 150 160 120 120 95 90 90 100 105 7 6 13.0 12.0 29.0 24.0 5.5 4.0 3.5 5.5 8.S 11.0 12.8 3.9 4.7 16.7 22.0 25.1 17.8 11.7 -30 —17 —54 —50 -48 —25 —14 —31 —51 -36* 8 S 3 o o o 2 *Jloati change in vascular resistance. P.or. = Aortic pressure in mm. Hg. Pi.v = Pulmonary vein pressure in mm. Hg. Q = Bronchial arterial flow in ml./min. Resistance (R) is calculated as P n o r .—PIT/Q. / \ B is the change in resistance. sac system sharply decreased the bronchial flow. Since the systemic blood pressure was unaffected in the latter case, it must be concluded that a marked increase in bronchial vascular resistance was induced (fig. 4). Serotonin Responses of the bronchial vascular resistance to serotonin (5-hydroxytryptamine) in doses of 1 ^g./Kg. into the bronchial artery were compared with the responses to injection of 5 ,u,g./Kg. into the pulmonary artery or vein (table 2). Bronchial Arterial, Injection. The systemic pressure remained unchanged after the injection of 1 /xg. of serotonin into the bronchial arterial system. The bronchial vascular resistance first showed a transitory increase followed in about 30 seconds by a decrease in resistance which persisted for approximately 2 minutes (fig. 5). Pulmonary Artery or Vein. The administration of 5 /xg./Kg. of serotonin into the pulmonary artery in 5 trials and .10 injections into the pulmonary veins resulted in a decrease in bronchial vascular resistance within about 10 seconds and reached a maximum in about 30 seconds and then returned to control values in about 2 minutes. The difference in response after injections into the bronehial artery and into the pulCirculation Research, Volume VIII, November 1960 BRONCHIAL ARTERIAL FLOW monary artery or vein are significant (p < 0.05, as calculated with the t test). 1153 FLOW Anatomic Control Downloaded from http://circres.ahajournals.org/ by guest on June 17, 2017 At the end of each experiment, the injection of 15 ml. of an 0.1 per cent solution of "fast green" dye into the aortic sac was used to demonstrate the vessels and tissues supplied by the bronchial artery. In the majority of the preparations, the bronchial vessels in both lungs were clearly outlined and the bronchial mucosa showed fair to very good staining. The bronchial arteries could be traced to the dorsal region of the bifurcation of the trachea. An annular vascular distribution of the dye could be seen between the tracheal rings for an inch or so of the trachea above the bifurcation. The major supply passed along the bronchi to the intrapulmonary tissues. The branches of the bronchial tree were clearly delineated. The va.sa vasorum of the pulmonary veins near the left atrium and of the pulmonary arteries near the heart were also filled. The connective tissue layer around the vagi was green in all preparations. With one exception, the pericardial vessels were also filled in all the cases where the dye had entered the bronchial vascular system. The wall of the esophagus was stained near the origin of the bronchial vessels around the aortic sac, despite the fact that all visible esophageal vessels had been li gated. Most of the cases also showed a slight filling of the right intercostal artery in the fourth or fifth interspace. The data of 2 preparations were not included in the present series because the bronchial vessels remained unstained. Discussion With the present preparation (fig. 1), the bronchial vascular resistance and blood flow can be studied in dogs under nearly normal hemodynamic conditions (fig. 2). The normal relations between the blood pressures and flows in the pulmonary and bronchial vascular systems are maintained. The preparation differs from normal in that the lungs are insufflated with positive pressure. The exact role of this factor has not yet been evaluated. Circulation Research, Volume VIII, November i960 20 10 0 MINUTES2 4 * * 9 Figure 3 Bronchial blood flow immediately after connection of flowmeter between aorta and vascular sac. The vertical width of the bar represents the oscillations of the float of the rotametcr. Prior to the establishment of the connection, the bronchial arterial flow had been disconnected for several minutes. The low resistance at this time is a characteristic response to the transitory occlusion, as in other vascular beds. After stabilization at S minutes, the insufflation pressure (1PPB) was raised from 20 to 30 cm. neater; this was accompanied by a fail in bronchial blood flow and a marked rise in bronchial vascular resistance. However, lowering of the insufflation pressure from 20 to 10 cm. water had no effect on the bronchial vascular resistance or blood flow. Since we used an insufflation pressure of 20 em. water for all of our studies, we assume that the bronchial vascular system was not significally affected by the use of our ventilatory device. The bronchial vascular resistance increased when the insufflation pressure was raised from 20 to 30 cm. water (fig. 3). It would thus appear that high intrapulmonary air pressures can affect the bronchial vessels, or perhaps the effect is by collapse of the pulmonary capillary bed into which some of the bronchial arterial flow passes. It would appear that the communication between the vascular beds of the bronchial and pulmonary arterial systems is not completely open for flow in both directions. This is suggested by the fact that a transitory HORISBERGER, RODBARD 1154 INJECTION INTO PA.(») OR PV.(e) £ mL/mln. 30 T I-OT • 1 O 0.8-• UJ "0.620 HI ADRENALIN INTO BRONCHIAL ART. INJECTION INTO BRONCHIAL ART. 10 1.0- Downloaded from http://circres.ahajournals.org/ by guest on June 17, 2017 uo.e o 8 0.61 ml/min. 30TS CONTROL 10 20 30 SECONDS 60 Figure 5 VASC. RESIST. T2 20 -I ESIST. ADRENALIN INTO THORACIC . AORTA 10 -I , 0 MINUTES I 2 3 Figure 4 (Above) Effect of adrenalin (l-epinephrine) on bronchial arterial blood flow (shaded area) and 'bronchial vascular resistance. After administration at 0- minutes, the resistance increased sharply at first; this was folloxoed by a transitory increase in flow as the resistance returned to normal. (Below) A reduction in calculated bronchial vascular resistance occurred on administration of adrenalin into the thoracic aorta as the systemic blood pressure increased; this ivas follotoed by a return to control values. Discussed in text. obstruction of the bronchial artery is followed by an increased flow. This may be interpreted as a reactive reduction in bronchial vascular resistance (hyperemia), a phenomenon which follows obstruction of the blood flow to tissues supplied by end-arteries. It is presumed that the accumulation of metabolic end-products generates a localized bronchial 90 Effect of serotonin. Changes from the normal calculated bronchial vascular resistance are indicated by the vertical axis. After injection into the bronchial artery (lower set of data), the resistance increased for about 15 seconds and then fell to normal or less than normal values. Injection into the pulmonary artery or vein produced a fall in bronchial vascular resistance which ivas maximal about 30 seconds after administration; the resistance values then returned to normal. arteriolar vasodilatation. The occurrence of such a vasodilatation may be interpreted as indicating that the blood passing through the pulmonary circulation does not eliminate these materials and the "reactive hyperemia." Since a portion of the bronchial arterial distribution is extrapulmonary, this part of the circulation obviously could not benefit by the intrapulmonary circulation, and part of the reactive hyperemia following release of occlusion of the bronchial vessels may be accounted for by vasodilatation in this extrapulmonary portion. An increase in insufflation air pressure would be expected to affect only the intrapulmonary portion of the bronchial vascular bed and not compress the extrapulmonary, mediastinal part in the open chest animal. Since the increase in airway pressure to 30 cm. water resulted in a substantial increase in bronchial vascular resistance (fig. 3), we can conclude that the intraCirculation Research, Volume VIII, November 1900 BEONCHIAL ARTERIAL PLOW Downloaded from http://circres.ahajournals.org/ by guest on June 17, 2017 pulmonary bronchial flow is responsible in a considerable part for these results. However, the injection of dye at the end of each experiment demonstrated a marked staining of the bronchial structures while only a small amount of the dye stained the extrapulmonary tissues in the mediastinum. Therefore, the flow to the mediastinal tissues probably accounts for only a small portion of the bronehial arterial flow. The effects seen after vagotomy (table 2) or after injection of Z-epinephrine directly into the bronchial artery (fig. 4) support the observations of Brunei- and Schmidt16 that the adrenergic fibers are vasoconstrictors to the bronehial vascular bed. One of the advantages of the present preparation is that it is possible to test the effect of drugs on the bronchial vascular system without interference with the systemic effects of these agents. This was demonstrated by a comparison of the effects of systemic injection of Z-epinephrine with those after injection into the bronchial vascular system (fig. 4). An immediate bronchial vasoconstrietion, shown by a reduction in flow, follows direct injection into the bronchial vascular system. After systemic injection of Z-epinephrine, the vasoconstrictor effects on the bronchial arterial system are delayed in accord with the time required for transit of the agent through the bypass and the flowmeter. It is of interest that an increased flow through the bronchial arterial system results prior to the arrival of the agent in the bronchial system. The slight decrease in calculated bronehial vascular resistance may be accounted for by a passive distention of the bronchial arteries and arterioles by the increased transmural pressure or by a reflex dilatation. Serotonin is considered to be a potent constrictor of the pulmonary vascular system.19 However, State et al.1 indicated an increase in collateral flow to the lungs after injection of large doses (1 to 10 mg.) of serotonin into the pulmonary artery. Some of this effect in their preparation may have reflected the considerable and prolonged coronary vasodilatation demonstrated by Maxwell et al.20 after Circulation Research, Volume VIII, November 1980 1155 the injection of serotonin in amounts of 20 /xg./Kg./min. It was, therefore, of interest to test the effect of serotonin in the bronchial artery; after injection of 1 /xg./Kg., a transient increase in resistance was followed by a decrease in resistance (table 2). Since'these small doses of serotonin did not significantly affect either the systemic or the pulmonary, arterial pressures, the demonstrated increase in bronchial flow can be explained only by vasodilatation of the bronchial arteries and arterioles. The response after injection into the pulmonary artery or vein shows that the bronchial vascular resistance fell sharply after a lag of about 10 seconds. Other data suggest that this effect may be a response to changes in pulmonary vascular resistance. Summary A method is described for the measurement of the collateral pulmonary blood flow in the thoracotomized dog by utilization of a flowmeter which measures flow into an aortic sac from which the bronehial arteries arise. This preparation maintains the normal perfusing pressures and diminishes phase changes in the-arterial pulse waves. The bronchial vascular'resistance is increased by an increase in the insufflation air pressure, by bilateral vasrotomy, or by the administration of lepinephrine into the bronchial arterial circulation. The bronchial vascular • resistance was decreased after a tratisitory interruption of the bronchial arterial blood flow (reactive hyperemia). After administration of serotonin in the bronchial artery, a transient increase in resistance was followed by a marked decrease. Intrapulmonary vascular injections produced on"y a decrease in resistance. The present data demonstrate the sensitivity of the preparation described. Summario in Interlingua Es deseribite un methodo pro le mesuration del collateral fluxo de sanguine pulmonar in le thoracotomisate can per medio de un fluxometro que mesura le fluxo entrante in un sacco aortic in le qual le arteriaa bronchial prende lor origine. Iste preparato mantene le normal pression de perfusion e reduce le alterationes de phase in le undas de pulso arterial. Le resistentia bronchio-vascular es augmentate per un augmento ia HORISBERGER, RODBARD 1156 le prcssion del aere insufflate, per vagotomia bilateral, o per le administration de (-epinephrina a in le circulation bronchio-arterial. Le resistentia broncho-vascular esseva reducitc post un interruption transiente del fluxo de sanguine bronchio-arterial (hyperemia reactive). Post le administration de serotonina a in le arteria bronchial, un transiente augmento del resistentia esseva scquite per un reduction de marcate magnitudes. Tnjeetiones vascular intrapulinonar produceva solmeiite un reduction del resistentia. Le presento dittos demonstra le sensibilitate del prepanito describite. Eeferences 1. STATE, D., SALISBURT, P. F., AND WEIL, P.: Downloaded from http://circres.ahajournals.org/ by guest on June 17, 2017 Physiologic and pharmacologic studies of collateral pulmonary flow. J. Thoracic Surg. 14: 599, 1957. 8. VON HALLER, A.: Icones anatom. fasc. I l l , p. 35-37, and Tab. art. bronchialis. Gottingen, 1756 (cf. reference 9). 9. KUTTNER: Beitrag zur Kenntniss der Kreislaufverhaltnisse der Saugethierlunge. Arch. path. Anat. 73: 476, 1878. 10. circulation to the lungs. Brit. J. Surg. 38: 97, 1950. 11. BERRY, J. L., BRAILSFORD, F. J., AND DALY, I. DEB.: Bronchial vascular system in the dog. Proc. Roy. Soc. London s.B 109: 214, 1931. 12. NOTKOVICH, H.: Anatomy of the bronchial arteries of the dog. J. Thoracic Surg. 33: 242, 1957. 13. MILLER, W. S.: The Lung. Springfield, III., Charles C Thomas, 1937. 14. 2. CUDKOWICZ, L., CALABBESI, M., NIMS, R. G., AND GRAY, F. D.: Simultaneous estimation of right and left ventricular outputs applied to a study of the bronchial circulation in dogs. Am. Heart J. 58: 732, 1959. 15. 16. BRUNER, H. D., AND SCHMIDT, C. F . : Blood flow in the bronchial artery of the anesthetized dog. Am. J. Physiol. 148: 648, 1947. 17. WILLIAMS, (). FlSHMAN, A . P . , TURINO, G. M., BRANDFONBRENER, M., AND HIMMELSTEIN, A.: "Effective" pul- monary collateral blood flow in man. J. Clin. Invest. 37: 1071, 1958. 7. O'MALLKY, C. D., AND SAUNDERS, J. B. DEC. M., Editors: Leonardo da Vinci on the Human Body: Anatomical Physiological, and Embryological Drawings of Leonardo da Vinci, with Translations, Emendations, and Biographical Introduction. New York, Henry Schuman, 1952, p. 394. M. H., JR., AND TOWBIN, E. J.: Magnitude and time of development of the collateral circulation to the lung after occlusion of the left pulmonary artery. Circulation Research 3: 422, 1955. 5. BLOOMER, W. E., HARRISON, W., LINDSKOO, G. E., AND LIEBOW, A. A.: Respiratory function and blood flow in the bronchial artery after ligation of the pulmonary artery. Am. J. Physiol. 157: 317, 1949. VIDONE, R. A., AND LIEHOW, A. A.: Anatomical and functional studios of the lung deprived of pulmonary arteries and veins, with application in the therapy of transposition of the great vessels. Am. J. Path. 33: 539, 1957. of the relation of pulmonary and bronchial circulation. .1. Exper. Med. 18: 500, 1913. C. Y.: Contribution of the bronchial circulation to the venous admixture in pulmonary venous blood (abstr. XIX). Intermit. Pli3-siol. Congross, 1953, p. 298. LIEBOW, A. A., HALES, M. R., HARRISON, W., BLOOMER, W., AND LINDSKOG, G. E.: Genesis and functional implications of collateral circulation of the lungs. Yale J. Biol. & Med. 22: 637, 1950. 3. GHOREYEB, A. A., AND KABSNER, H. T.: Study 4. PALY, M. DEB., AVIADO, D. M., JR., AND LEE, COCKETT, F. B., ANDVASS, C. C. N.: Collateral 18. DAMERON, J. T., AND GREENE, D. G.: Use of the Burns valve as a simple respirator for intrathoracic surgery in the dog. J. Thoracic Surg. 20: 706, 1950. 19. PAGE, I. H.: Cardiovascular action of serotonin (5-hydroxytryptaminc). Proc. Symposium on 5-hydroxytrayptamine, London, April, 1957. New York, Pergamon Press, 1957, pp. 93-108. 20. MAXWELL, G. M., CASTILLO, C. A., CLIFFORD, J. E., CRUMPTON, C. W., AND ROWE, G. E.: Effect of serotonin (5-hydroxytryptamine) on the systemic and coronary vascular bed of the dog. Am. J. Physiol. 197: 736, 1959. Circulation Research, Volume VIII. November I960 Direct Measurement of Bronchial Arterial Flow BRUNO HORISBERGER and SIMON RODBARD Downloaded from http://circres.ahajournals.org/ by guest on June 17, 2017 Circ Res. 1960;8:1149-1156 doi: 10.1161/01.RES.8.6.1149 Circulation Research is published by the American Heart Association, 7272 Greenville Avenue, Dallas, TX 75231 Copyright © 1960 American Heart Association, Inc. All rights reserved. Print ISSN: 0009-7330. 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